Download The development of alarm call behaviour in mammals and birds

Animal Behaviour 78 (2009) 791–800
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Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
The development of alarm call behaviour in mammals and birds
Linda I. Hollén*, Andrew N. Radford
School of Biological Sciences, University of Bristol
a r t i c l e i n f o
Article history:
Received 28 July 2008
Initial acceptance 29 September 2008
Final acceptance 23 July 2009
Published online 27 August 2009
MS. number: 08-00493R
Keywords:
alarm calling
assessment–management
call production
call responses
call usage
development
information transfer
learning
maturation
vocal communication
Alarm calling is a widespread antipredator behaviour. Although the function and evolution of alarm call
behaviour have long been studied in detail, only in the last decade has there been an upsurge in research
into its development. Here, we review the literature on the development of alarm call production (the
delivery of calls with a specific set of acoustic features), alarm call usage (the use of calls in particular
contexts) and alarm call responses (the responses to calls produced by others). We detail the mechanistic
processes that may underlie the development of each aspect, consider the selection pressures most likely
to explain the relative importance of these processes, and discuss the substantial variation in developmental rates found both between and within species. Throughout, we interpret existing findings about
age-related differences in alarm call behaviour from two major communicatory viewpoints: the idea that
signals carry information from sender to receiver, with young taking time to acquire adult-like skills; and
the possibility that signals are used to manage the behaviour of receivers, with young behaving adaptively for their age. We conclude that a broader use of various techniques (e.g. cross-fostering and
temporary removals), the formation of stronger collaborative links with other disciplines (e.g. physiology
and neurobiology) and the initiation of new research avenues (e.g. kleptoparasitism) will ensure that
studies on the development of alarm call behaviour continue to enhance our understanding of such
topics as the evolution of communication and language, kin selection and cognitive processing.
Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Alarm calling, the giving of particular vocalizations in the face of
impending danger, is a key antipredator strategy that has evolved
in a wide range of species (Caro 2005). Alarm call behaviour, as with
all vocal communication, comprises three aspects: the delivery of
calls with a specific set of acoustic features (call production); the
use of calls in particular contexts (call usage); and the response to
calls produced by others (call responses). Although there is often an
obvious selfish selection pressure on receivers to respond to alarm
calls (they may be more likely to survive if they do), their
production can appear altruistic: in giving a signal that enhances
the likelihood of others escaping, callers may attract the attention
of the predator themselves. Studies of alarm call behaviour have
therefore proved invaluable for our understanding of such issues as
kin selection, nepotism, reciprocal altruism and cooperation
(Sherman 1977; Hoogland 1996; Krams et al. 2006; Wheeler 2008).
Similarly, research into alarm calling has provided many insights
into the cognitive processes underlying signal perception (Blumstein 1999) and the evolution of communication (Spinozzi 1996;
Evans & Evans 2007), including human language (Kuhl 1994;
Werker & Yeung 2005). Clearly, therefore, alarm call behaviour is of
* Correspondence: L. I. Hollén, School of Biological Sciences, University of Bristol,
Woodland Road, Bristol BS8 1UG, UK.
E-mail address: [email protected] (L.I. Hollén).
interest and relevance to researchers in many fields, and so it is not
surprising that such a large literature exists on the subject
(reviewed in Caro 2005).
Until recently, that literature had contained relatively few
studies focusing on the development of alarm call behaviour. One
likely explanation for the paucity of such research is the difficulty of
acquiring the relevant data: alarm calling by young often occurs
relatively rarely and unpredictably, and a long time is needed to
determine fully the developmental trajectories present within
a species. However, the establishment of many more long-term
field studies and innovation from scientists, particularly in the last
decade, has led to a rapid rise in research into the development of
alarm call behaviour in both mammals and birds (Table 1). This
increase in research interest is welcome, because developmental
studies can inform us about the importance of various selection
pressures, such as local environmental conditions (Lima & Dill
1990; Berger et al. 2001), can help elucidate the relative importance
of kin selection, reciprocal altruism and direct benefits (Sherman
1977), and can provide valuable insights into functional signalling
and thus the evolution of communication (Kuhl 1994; Blumstein
1999). Studies investigating the development of alarm call behaviour also provide an excellent opportunity to compare two conflicting viewpoints that have arisen with respect to animal
communication: that signals are used to transfer information
0003-3472/$38.00 Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2009.07.021
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L.I. Hollén, A.N. Radford / Animal Behaviour 78 (2009) 791–800
Table 1
Studies examining the development of alarm call behaviour in mammals and birds
Species
Aspect*
Methody
Source
Summary
Mammals
Belding’s ground squirrel,
Spermophilus beldingi
U
R
O & E (LP)
E (PB)
Robinson 1981
Mateo 1996a, b
R
E (PB)
R
E (LP, MP)
Mateo & Holmes 1997,
1999a, b
Hanson & Coss 1997
R
E (PB)
Hanson & Coss 2001b
R
E (MP, PB)
Wilson & Hare 2006
R
E (PB)
Schwagmeyer & Brown 1981
Juveniles do not discriminate between predators and nonpredators
Young can discriminate between calls (measured by heart rate)
before emergence, but responses become adultlike before
dispersal at 7 weeks
Early rearing environment and exposure to dams affect the rate of
response development
Juveniles show more urgent responses to chatters (terrestrial threat)
and less urgent responses to whistles (avian threat) compared to adults
Compared with adults that treat a hawk as a more immediate
threat than a dog, juveniles treat both with equivalent urgency
Like adults, juveniles respond to ultrasonic alarm signals by increasing
their vigilance
Juveniles are more likely not to respond to certain alarm
calls than adults
Alarm calls of young are higher pitched than those of adults
California ground squirrel,
Spermophilus beecheyi
Richardson’s ground squirrel,
Spermophilus richardsonii
Thirteen-lined ground squirrel,
Spermophilus tridecemlineatus
Yellow-bellied marmot,
Marmota flaviventris
Great gerbil, Rhombomys opinus
Pika, Ochotona princeps
P
O
Blumstein & Munos 2005
P
U
E (MP, PB)
O
Randall et al. 2005
Ivins & Smith 1983
Goeldi’s monkey, Callimico goeldi
R
E (PB)
Masataka 1983a
Squirrel monkey, Saimiri sciureus
R
E (MP, PB)
Herzog & Hopf 1984
R
E (PB)
McCowan et al. 2001
P, U, R
O & E (PB)
Seyfarth & Cheney 1980, 1986
R
O & E (PB)
Hauser 1988
Japanese macaque, Macaca fuscata
R
O & E (PB)
Masataka 1983b
Bonnet macaque, Macaca radiata
R
E (PB)
Ramakrishnan & Coss 2000
Barbary macaque, Macaca sylvanus
Chacma baboon,
Papiocynocephalus ursinus
R
R
O & E (PB)
E (PB)
Fischer et al. 1995
Fischer et al. 2000
Verreaux’s sifaka, Propithecus
verreauxi verreauxi
Meerkat, Suricata suricatta
R
E (PB)
Fichtel 2008
P
O
Hollén & Manser 2007a
U
O
Hollén et al. 2008
R
O & E (PB)
Hollén & Manser 2006
R
E (PB)
Miller & Blaich 1986
R
E (PB)
Miller et al. 1990
Laughing gull, Larus atricilla
R
O & E (PB)
Impekoven 1976
Common cuckoo, Cuculus canorus
R
E (PB)
Davies et al. 2006
Dunnock, Prunella modularis
R
E (PB)
Davies et al. 2004
Robin, Erithacus rubecula
R
E (PB)
Davies et al. 2004
Reed warbler, Acrocephalus scirpaceus
R
E (PB)
Davies et al. 2004
Pied flycatcher, Ficedula hypoleuca
R
E (PB)
Korneeva et al. 2006
White-browed scrubwren,
Sericornis frontalis
R
E (PB)
Maurer et al. 2003
R
E (PB)
Platzen & Magrath 2005
R
E (PB)
Magrath et al. 2006
R
E (PB)
Rajala et al. 2003
Vervet monkey, Chlorocebus aethiops
Birds
Mallard, Anas platyrhynchos
Willow tits, Parus montanus
Calls of pups and subadults are higher pitched than those of adults
Young give calls at similar rate and duration in both predator
and nonpredator contexts
The responses of young (alarm calling and/or freezing) bear no
resemblance to adult responses
Responses of socially isolated young resemble responses
of mother-reared infants
Infants gradually develop an adult-like response to alarms over the
first year of life
Much of the adult repertoire is recognizable in calls of young infants
Young are predisposed to use calls correctly but need refinement
Responses develop entirely as the result of experience
Responses are affected by the exposure rates of superb starling
alarm calls
1-year-old infants rarely respond to alarm calls, 2-year-olds respond
to any stimulus, whereas responses of 3-year-olds are similar
to those of adults
No marked difference between adults and juveniles when responding
to adult alarms, but juveniles more likely to flee to juvenile alarms
Juveniles generally show stronger responses than adults
At 2.5 months infants fail to respond whereas at 4 months
they respond irrespective of call type. At 6 months they show
adult-like responses
Young infants flee towards adults and only show adult-like responses
at 6 months (physical independence)
Calls of young are higher pitched and of longer duration than those
of adults
Young alarm call more in response to nonthreatening species
compared to adults
Newly emerged young flee down burrows irrespective of call
type and approach adult-like responses over the following 6 months
Birds older than 48 h show lower levels of freezing than younger
birds in response to maternal alarm calls
Socially reared devocalized ducklings show greater levels of freezing
than socially isolated devocalized ducklings
Responsiveness to alarm calls is affected by prenatal exposure
to these calls
Cuckoo chicks show innate pretuning to their host species’ alarms,
but need exposure to calls for the silent gaping response to develop
Cross-fostered nestlings still respond specifically to their own species’
alarms but less strongly than normally raised nestlings
Cross-fostered nestlings still respond specifically to their own species’
alarms but less strong than that of normally raised nestlings
Cross-fostered nestlings still respond specifically to their own species’
alarms but less strong than that of normally raised nestlings
Defensive behaviour develops as the auditory sensitivity to certain
frequencies matures
Nestlings acquire the ability to respond appropriately to alarm calls
late in the nestling period
Nestlings react more strongly to calls posing greater danger,
appropriate to their stage of development
Young respond appropriately to aerial alarm calls coinciding with
becoming vulnerable to aerial attack
Juveniles are more likely than adults to flee after hearing conspecific
alarm calls
L.I. Hollén, A.N. Radford / Animal Behaviour 78 (2009) 791–800
793
Table 1 (continued )
Species
Aspect*
Methody
Source
Summary
Great tits, Parus major
R
E(PB)
Rydén 1978a, b
R
E (PB)
Rydén 1980
R
E (MP)
Kullberg & Lind 2002
R
E (PB)
Madden et al. 2005
Young only develop a response to aerial alarm calls late in the
nestling period
Nestlings raised in an environment dominated by high-pitched
sounds subsequently show a decreased responsiveness to aerial
alarm calls (high pitched)
Naı̈ve fledglings do not respond differently to a model of a predator
than to a model of a nonpredator
Chicks do not develop a response to their foster species’ alarms
R
E (PB)
Madden et al. 2005
Chicks do not develop a response to their foster species’ alarms
Red-winged blackbird,
Agelaius phoeniceus
Brown-headed cowbird,
Molothrus ater
The aspect of alarm call behaviour that was investigated: P ¼ production; U ¼ usage; R ¼ responses.
The method used to investigate the development of alarm call behaviour: O ¼ observations (including natural sound recordings of alarm calls); E ¼ Experiments (LP ¼ live
predator presentation; MP ¼ model predator presentation; PB ¼ playbacks; where playbacks were used, natural sound recordings or predator presentations used to collect
alarm calls for the experiments are not included).
*
y
between senders and receivers, and that they are used to manage
the behaviour of receivers.
Ever since the seminal work demonstrating that vervet
monkeys, Chlorocebus aethiops, produce acoustically distinct alarm
calls to various predators, and that receivers respond in different,
adaptive ways to them (Seyfarth & Cheney 1980, 1986), numerous
studies have concluded that alarm calls include information about
the urgency of the threat and/or the type of predator (Macedonia &
Evans 1993; Manser 2001; Leavesley & Magrath 2005). Consequently, alarm calling has often been deemed referential, that is,
conveying encoded information to receivers about objects and
events in the external environment (Evans 1997), and this
linguistically inspired, meaning-based view of vocal communication has become the predominant way of thinking. However, some
researchers argue that the ‘information transfer’ perspective is
problematic: it implies a cooperative venture between sender and
receiver, which need not be the case; and, by proposing that the
acoustic structure of calls bears no relation to their function, it adds
an unnecessary level of complexity to the process (Owings &
Morton 1998; Owren & Rendall 2001). A more fundamental
standpoint focuses on call structure rather than call meaning.
According to this ‘assessment–management’ view, callers use
vocalizations to elicit affective responses in others, thereby altering
the behaviour of these individuals to the caller’s advantage, but not
necessarily that of the receiver (Owings & Morton 1998). Receiver
responses can be unconditioned, being produced directly by the
energy in the signal itself, or conditioned, resulting from past
interactions where the signal was coupled with a certain reaction
(Owren & Rendall 2001).
From the information transfer perspective, young individuals
have to develop the ability to encode correct information in the
acoustic structure of alarm calls, to provide the correct information
through their use of calls, and to decode information provided by
the alarm calls of others. From the assessment–management
perspective, the behaviour of young individuals must be understood in terms of their current needs: young will produce, use and
respond to alarm calls in a way that is functional and adaptive for
their particular developmental stage and that helps them cope
with age-dependent risks. We believe that both approaches have
merit, and that they are not necessarily mutually exclusive: young
animals have both to survive their current environment and,
simultaneously, anticipate future conditions. Here, we therefore
interpret existing findings on the development of alarm call
behaviour in light of both viewpoints. We consider alarm call
production, usage and responses in turn, although it is worth
noting that far more is currently known about the latter (Table 1).
For each aspect we review the existing literature, considering the
relative importance of, and evidence for, the different mechanistic
processes (genetic predispositions, physical and neurological
maturation, physiological changes and learning) that may separately or in combination underlie the development of behaviour,
and suggest under what ecological and social situations each might
be most likely to play a role. We also discuss the substantial variation in developmental rates found both between and within
species. Throughout the review we provide suggestions about the
broader use of established techniques, potentially fruitful collaborations with other disciplines and ideas for future research
directions, with particular emphasis on how these might help to
tease apart, or reconcile, ideas about information transfer and
assessment–management.
DEVELOPMENT OF ALARM CALL PRODUCTION
Early research concluded that alarm calls are fully formed in
structure at first appearance in the vocal repertoire. For example,
Seyfarth & Cheney (1980, 1986) described the alarm calls first given
by infant vervet monkeys as acoustically indistinguishable from
adult calls. However, the great majority of studies reporting no
modification of alarm calls during development were conducted
more than two decades ago when sophisticated analytical tools
were not available (reviewed in Seyfarth & Cheney 1997). Rather
than visually examining spectrograms to quantify the similarity of
sounds, researchers nowadays process acoustic signals using
automated digital techniques (e.g. Baker & Logue 2003). Probably as
a result, recent studies have shown that alarm calls do show some
plasticity. In yellow-bellied marmots Marmota flaviventris (Blumstein & Munos 2005), great gerbils, Rhombomys opinus (Randall
et al. 2005) and meerkats, Suricata suricatta (Hollén & Manser
2007a), for example, the alarm calls of young are higher pitched
than those of adults. The alarm calls of young meerkats are also
longer in duration, more modulated, noisier and have their main
energy at higher frequencies than those of adults (Hollén & Manser
2007a). Hence, although young produce alarm calls that resemble
the general structure of adult calls, there are often discernible
differences.
One possible reason for these age-related differences is that
there has been strong selection pressure for juvenile alarm calls to
be inherently more alerting or ‘plosive’ than those of adults,
because of the higher vulnerability of young individuals to predation (Holmes 1984). Particular sounds stimulate brainstem circuitry
directly and induce changes in the attention, arousal, motivation or
emotion of the receiver (Eaton 1984; Owren & Rendall 2001), so by
producing alarm calls of a certain structure young might manage
the behaviour of nearby adults in a way that reduces the risk to the
young themselves. This might explain why, for example, the alarm
calls of juvenile yellow-bellied marmots cause adults to suppress
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L.I. Hollén, A.N. Radford / Animal Behaviour 78 (2009) 791–800
their foraging and increase their vigilance to a greater extent than
the alarm calls of other adults (Blumstein & Daniel 2004). Receivers
need not necessarily benefit from a manipulation of their behaviour
(Owren & Rendall 2001), but because calls from juvenile marmots
are likely to be produced by offspring or other young relatives in
a matriline, enhancing the detection of predators and thus
increasing the survival likelihood of the caller would, in this case,
also provide kin-selected benefits to the adults involved (Blumstein
& Daniel 2004).
To investigate the potentially plosive nature of alarm calls
requires detailed acoustic analyses, focusing on features such as
sharp onsets and dramatic frequency and amplitude modulations
that are known to elicit affective responses in receivers (Owren &
Rendall 2001). If the inherent structure of an alarm call is important, we would predict that such characteristics are more apparent
in those calls that result in a stronger response. To confirm the
relative salience of different acoustic parameters, computersynthesized calls could be played back to the target animals.
Playbacks of such manipulated calls have yet to be used in the
investigation of alarm call development, but have been successfully
used in other contexts (Masataka 1983a; Reby et al. 2005). In
Goeldi’s monkeys, Callimico goeldi, for example, researchers altered
particular frequency and temporal features of adult alarm calls and
played them back to other adult group members (Masataka 1983a).
Receiver responses changed distinctly with an increase of only
0.2 kHz in the frequency range, whereas there was no discernible
effect of variants of duration, centre frequency and bandwidth (the
kind of features that do not necessarily have an impact on nervous
systems). This method could therefore be useful in determining not
only the importance of particular acoustic parameters, but also the
scale of acoustic differences needed to evoke different receiver
responses.
Age-related differences in alarm call production need not
necessarily be adaptive, but might instead be the consequence of
developmental constraints. The most obvious possible constraint
on juvenile call production is physical maturation. For example,
fundamental and peak frequency-related parameters, which
determine call pitch, are likely to change as the length of the vocal
tract and the size of the resonance cavities increase during growth
(Fitch & Hauser 1995). Vocal control also improves as individuals
grow older (Boliek et al. 1996; Scheiner et al. 2002), possibly
explaining why noisy call types which require relatively little
control over the vocal apparatus (Lieberman 1986) are often those
that are produced during the first days of life (e.g. Hollén et al.
2008). Although the research focus to date has been on motor
constraints, neurological development in the relevant brain areas
might prove equally crucial. Unfortunately, whereas the neural
basis of birdsong has long been established and much has been
discovered about how different brain nuclei and their connecting
pathways contribute to song learning (reviewed in Bottjer & Arnold
1997; Brainard & Doupe 2002; Nottebohm 2005), very little is
known about the neural mechanisms underlying alarm calling. We
do know that certain brain structures play a key role in the
development of antipredator defence behaviour (Wiedenmayer
2009), but there is an urgent need for insight into how alarm calls
are encoded neurologically and how neural changes relate to agespecific changes in alarm call production.
Acoustic differences in the alarm calls produced by different age
groups might also arise if physiological arousal levels differ (see
Hanson & Coss 2001a). Changes in arousal have been shown to
influence parameters such as pitch and duration in nonalarm calls
(Scheiner et al. 2002; Rendall 2003), and juveniles may be more
aroused because they are generally more vulnerable (Holmes
1984). Valuable light could be shed on this possibility by measuring
some indicator of arousal, such as heart rate, at the time of an alarm
call (see Rydén 1980; Evans & Gaioni 1990; Mateo 1996a). Assessment of glucocorticoid concentrations in faeces (e.g. Blumstein
et al. 2006) could also help to establish whether different age
groups display baseline differences in arousal and whether this
affects their production of alarm calls. In some species, elevated
corticoids can also facilitate learning and memory (Hanson & Coss
2001a; McGaugh 2004), so future work should explore whether an
increase in arousal could function to promote acquisition of alarm
call behaviour rather than being the direct cause itself (see Mateo
2006).
Inherent differences in the anatomy, neurology or physiology of
individuals of different ages might result in juvenile calls that are
less plosive or, if the transfer of information is important, that
denote something less threatening than those produced by adults.
This would help to explain such findings as the reduced flight
response and slower reaction times of adult vervet monkeys,
bonnet macaques, Macaca radiata, and California ground squirrels,
Spermophilus beecheyi, to juvenile alarm calls compared to those of
other adults (Seyfarth & Cheney 1980; Ramakrishnan & Coss 2000;
Hanson & Coss 2001b); given the greater vulnerability of young, it
seems unlikely that there will have been adaptive selection on
juvenile calling to be less evocative than that of adults. In other
species, developmental constraints might result in juvenile alarm
calls that are less informative than those of adults. For example, if
adult yellow-bellied marmot calls really do signal threat urgency
(Blumstein & Armitage 1997), perhaps juvenile calls only suggest
the general presence of predators. The increased vigilance by adult
receivers in response to juvenile alarm calling (Blumstein & Daniel
2004) might therefore be because there is a greater need for private
assessment of the current risk compared to when another adult has
called.
A further consequence of differences in the structure of calls
produced by adults and juveniles is that receivers might be able to
identify callers of different age classes (Blumstein & Daniel 2004).
Any difference in response might therefore arise, not because of
induced reactions to particular acoustic characteristics or because
of differences in the information content of the call itself, but
because the receiver has chosen to respond differently depending
on the identity of the caller. For example, because juveniles are
potentially less reliable at providing accurate information, for
example they might detect predators less frequently or make more
mistakes in their use of alarm calls (see Development of alarm call
usage), receivers might choose to respond less strongly to them
(e.g. Hanson & Coss 2001b) or, alternatively, they might increase
their vigilance more in response to juvenile alarm calling (e.g.
Blumstein & Daniel 2004) to obtain a suitably accurate assessment
of the current predation risk.
There is some evidence that adult receivers are capable of
discriminating between reliable and unreliable callers in general
(Hare & Atkins 2001; Blumstein et al. 2004), but no studies have yet
examined whether relative reliability is actually an important
reason why receivers respond differently to adult and juvenile
alarm callers. To do so, calls and contexts could be artificially
manipulated: the perceived reliability of different individuals could
be altered by pairing their alarm calls with or without model
predators, with subsequent assessment of receiver responses (see
Hare & Atkins 2001; Blumstein et al. 2004). Moreover, because
juveniles do not necessarily appear capable of distinguishing
between reliable and unreliable callers (Robinson 1981; Ramakrishnan & Coss 2000), similar experiments could be used to
determine when such discrimination ability develops. By
combining manipulations of perceived reliability with the playback
of synthezised calls (see above) it would be possible to begin
teasing apart the relative importance of inherent call characteristics
and any potential information contained within them, as well as
L.I. Hollén, A.N. Radford / Animal Behaviour 78 (2009) 791–800
establishing why juvenile alarm calls are more evocative than adult
calls in some species, but less so in others.
DEVELOPMENT OF ALARM CALL USAGE
A prerequisite for effective alarm call usage is the recognition of
predators (reviewed in Caro 2005). There is compelling evidence
that some species are capable of recognizing predators when they
are first encountered (Curio 1993; Veen et al. 2000; Göth 2001).
Such recognition might be innate, but this may often be hard to
demonstrate because other processes could play a role before the
behaviour is first expressed and can thus be measured. For
example, amphibians can learn to recognize future predators while
in the egg (Ferrari & Chivers 2009), human babies can learn to
distinguish sounds while in utero (Chamberlain 1998), and the
young of species that spend the first few weeks of life underground
may have had some exposure to the sounds of predators and
conspecifics prior to emergence (Mateo 1996a). A fixed unlearned
recognition ability on first exposure to predators has the advantage
that individuals stand a better chance of escaping when they are
most vulnerable early in life, but may not allow spatial or temporal
flexibility to new or changing circumstances. However, if a species
is, for example, preyed on by an especially dangerous predator and
postattack survival is highly unlikely, the advantage of showing
appropriate initial behaviour will clearly outweigh the disadvantage of a lack of plasticity.
Most studies showing seemingly unlearned predator recognition have been on species where young live independently from the
moment of hatching (e.g. Brown & Warburton 1997; Burger 1998;
Göth 2001). However, in those with parental care, it often appears
as if individuals come to recognize predators over time (Maloney &
McLean 1995; Hanson & Coss 1997; Griffin et al. 2000, 2001). The
consistent pattern from these studies is that cues from experienced
conspecifics trigger learning about predators (Griffin et al. 2000).
Behaviour that requires time to perfect may result in an increased
chance of errors when a predator is first encountered, but allows
fine tuning to particular conditions: individuals can adjust their
behaviour if predation risk varies in space and time, if they become
exposed to previously unfamiliar predators, or if vulnerability to
predation alters with age (Lima & Dill 1990; Warkentin 1995;
Berger et al. 2001).
Compared to the development of predator recognition, very
few studies have so far been conducted on the development of
alarm call usage (see Table 1), but they have all reached similar
conclusions. As with other call types (see e.g. Seyfarth & Cheney
1986; Hauser 1989), young seem predisposed from birth to use
specific alarm calls in generally appropriate contexts, but they
often give them to a broader range of species than adults (Seyfarth & Cheney 1980; Hollén et al. 2008). One possible explanation for this is that smaller individuals are preyed on by more
predator types than adults and so young are using alarm calls in
a way that is appropriate for their developmental stage (see
Owings & Morton 1998). By alarm calling to a predator that
threatens them, but not adults, young may be attempting to elicit
a response that benefits the caller but that has no direct immediate benefit to the receiver; the alarm call is not necessarily
acting as a warning to enhance the adult receivers’ own safety. To
date, only one study has provided suitable empirical data to test
this assessment–management prediction. Hollén et al. (2008)
compared the predator species that elicited alarm calls from
meerkats of different ages and found that stimuli posing a greater
threat to young than to adults do not elicit more calling from the
former. These findings argue against age-related changes in
vulnerability as the sole explanation for developmental changes
in alarm call usage, at least in this species.
795
Rather than being age adaptive, young might alarm call to
a greater number of species than adults because they make more
errors. For example, Seyfarth & Cheney (1980) showed that alarm
calls normally given by adult vervet monkeys to threatening stimuli
are often uttered by young in response to nondangerous stimuli,
such as doves (Streptopelia sp.), falling leaves or warthogs, Phacochoerus africanus, although these overgeneralizations are not
entirely random: infants give ‘leopard’ alarms primarily to terrestrial mammals, ‘eagle’ alarms to objects in the air, and ‘snake’
alarms to snakes or long thin objects on the ground. As they grow
older, vervets restrict their calling to particular predator species
within these general classes. Although little is known about the
neurological basis of alarm calling (see above), it could be that the
increased vulnerability of young results in nervous systems and
brain structures that are more sensitive to external stimulation
than those of adults (Wiedenmayer 2009). The threshold for calling
might therefore be lower in young, resulting in the production of
alarm calls in contexts that would not elicit adult calling; development of adult-like call usage might therefore arise because of
neurological maturation.
Alternatively, adult-like call usage might develop through
increased experience with predator encounters and the alarm calls
of others: individuals could learn to make fewer mistakes and
become better at conveying the correct information. By hearing
others use specific calls only in certain contexts, young could learn
by association. There is also some evidence that adults might
reinforce correct alarm call usage by juveniles. For example, adult
vervet monkeys are more likely to give second alarm calls when
infants alarm call to known predators than to nonpredators (Seyfarth & Cheney 1980), although no data are available on whether
this leads to more rapid development. Moreover, if reinforcement
does play a role, it may be inadvertent from an adult’s perspective
because they are equally likely to give second alarms following
a correct alarm call by another adult as they are following a correct
alarm call by a juvenile (Seyfarth & Cheney 1986). So, while adult
responses may facilitate learning of correct alarm call usage, adults
do not appear actively to teach infants in this context (Thornton &
Raihani 2008).
Although there is some evidence for the involvement of
learning, more studies are needed to determine the extent to which
it drives the development of alarm call usage. In this regard, crossfostering of young could be important. Research into the use of
nonalarm calls by rhesus, Macaca mulatta, and Japanese, Macaca
fuscata, macaques found that the normal striking species difference
in calling was generally retained by cross-fostered individuals: they
mostly adhered to their own rather than their adopted species’ call
usage, suggesting a strong unlearned component to this behaviour
(Owren et al. 1993). To date, cross-fostering studies of alarm call
behaviour have focused solely on the development of responses
(see below). However, it is a method that could easily be used to
tease apart the processes affecting the development of alarm call
usage, especially in combination with call playbacks or presentations of live predators, stuffed models or predator deposits, such as
urine, faeces and hair (see Kullberg & Lind 2002; Hollén & Manser
2007b). In general, the use of such experiments also provides an
excellent means of increasing the sample size for infrequently and
randomly occurring events, one of the problems with studying
alarm call behaviour in natural populations.
DEVELOPMENT OF ALARM CALL RESPONSES
Young of many species respond to alarm calls seemingly on their
first exposure to them. For example, only 24 h posthatching,
mallard ducklings, Anas platyrhynchos, show a high degree of
freezing upon hearing maternal alarm calls (Miller & Blaich 1986).
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Similarly, on their first day of emergence from the natal burrow,
juvenile Richardson’s ground squirrels, Spermophilus richardsonii,
respond to ultrasonic alarm calls by increasing their vigilance
(Wilson & Hare 2006), and juvenile Belding’s ground squirrels enter
the burrow or freeze when they hear conspecific alarm calling
(Mateo 1996b). Such responses might be a simple consequence of
the inherently plosive acoustic properties of alarm calls (see
Development of alarm call production). Alternatively, because an
early ability to respond appropriately to alarm calls increases the
likelihood of survival, and trial-and-error learning in a predatory
context can be fatal, there should have been strong selection
pressure for unlearned responses to alarm calls (Lind & Cresswell
2005). Young animals may therefore be born with the capacity to
respond appropriately to alarm calls because evolutionary
processes have fixed these traits in their behavioural repertoire
(Blumstein 2006).
The exact response to alarm calls need not, however, remain
fixed throughout life: in many species, changes in behaviour
become apparent over a period of days, weeks or even months
(Seyfarth & Cheney 1986; Mateo 1996b; Fischer et al. 2000;
McCowan et al. 2001; Platzen & Magrath 2005; Hollén & Manser
2006; Fichtel 2008). For example, in the few days after first emergence from the burrow, juvenile Belding’s ground squirrels become
more selective and begin to respond more distinctly to alarm calls
compared to nonalarm calls, to which they initially react in the
same way. Three weeks later, their behaviour has further changed,
although compared to adults they still freeze less, stay alert longer
and run to the burrow more often (Mateo 1996b). In meerkats,
young pups flee to a burrow in response to all alarm calls, but later
respond differently depending on the urgency of the threat (Hollén
& Manser 2006). Natural selection may favour unspecific responses
early in life when avoiding predation is of paramount importance
(food is provided by others), but refinement is needed to minimize
the cost of unnecessary time and energy expenditure later in life: if
the threat is not imminent, valuable foraging time will be lost by
running to a burrow (Sih 1997; Lima 1998). Even seemingly
unlearned responses may therefore be reorganized during development (Wiedenmayer 2009).
One possible explanation for a change in alarm call responses
with increasing age is a change in vulnerability. For example, young
white-browed scrubwren, Sericornis frontalis, nestlings are at risk
from ground predators, but aerial predators pose little danger to
them inside their enclosed nest. This might explain why young
nestlings only suppress their calling in response to the playback of
alarm calls signalling the presence of a ground predator, but not
those signifying an aerial threat; the responses of nestlings are age
adaptive (Platzen & Magrath 2005). Supporting this idea, the same
authors later showed that scrubwren fledglings, which are at risk
from aerial predators, fall silent immediately after playback of their
parent’s aerial alarm calls (Magrath et al. 2006). The development
of responses to aerial and ground alarm calls in these birds shows
striking similarities with the development of responses to such
alarm calls in ground squirrels and mongooses (Mateo 1996b;
Hanson & Coss 1997, 2001b; Hollén & Manser 2006), suggesting
that age-adaptive developmental trajectories may be widely
applicable across a broad range of species (see Alberts & Cramer
1988; Owings & Morton 1998).
An alternative explanation for differences in alarm call
responses by individuals of different ages is that responses of young
are not fully functional early in development. One reason for this
might be constraints imposed by immature sensory or motor
systems. For example, young red deer, Cervus elaphus, calves are
limited in their capacity to run because of their low body weight:
until their physical development reaches a certain point, they may
be forced to respond to alarm calls by becoming immobile, rather
than fleeing (Espmark & Langvatn 1985). Brain areas such as the
amygdala, the hippocampus and the prefrontal cortex, which form
the ‘fear circuit’ and support defensive behaviour in general, may
also lack full functionality early in life (reviewed in Wiedenmayer
2009). During development, new neurons will generate and
differentiate (Berdel & Morys 2000), synaptic transmissions will
change (Thompson et al. 2008), connections between different
brain areas will mature (Rinaman et al. 2000), and hormones that
are important for the activation of the fear circuit will be secreted
(Moriceau et al. 2006). Although the consequences of neurological
development on alarm call behaviour are poorly understood, it is
highly plausible that these changes could alter the functional
output of the fear circuit, and thus alarm call responses, by
promoting or inhibiting certain behaviours. Processes independent
of a direct interaction with either the predatory threat or alarm calls
themselves can therefore contribute to differences in responses
between age groups.
Although some changes in alarm call responses with age might
be the result of unfolding maturation, early experience may also
shape the behaviour of young by influencing the development of
their perceptual, central or motor systems. There is good evidence
that both social experience (Arakawa 2007) and maternal care
(Champagne & Curley 2005) influence general defensive behaviour
in juveniles, and both could feasibly play a role in the development of alarm call responses. For example, rearing conditions have
been shown to affect the development of alarm call responses in
rodents, with captive juvenile Belding’s ground squirrels more
likely to run to a refuge and to stay alert for longer than those
raised in the wild (Mateo & Holmes 1999a). Moreover, captivereared young started discriminating between different alarm calls
later in life compared to their wild counterparts, and the authors
suggested this was because pups in captivity were exposed to
higher levels of auditory stimulation in their burrows. The
permanent absence of mothers after weaning also delays the point
at which wild juvenile Belding’s ground squirrels respond differently to alarm and nonalarm calls (Mateo & Holmes 1997).
However, future studies need to disentangle the importance of
missing maternal care from a lack of opportunities for social
learning (see below).
Young animals might also become more adult-like in competence, making fewer mistakes and responding more appropriately
to alarm calls, through learning. Animals can learn how best to
respond through direct interaction with alarm calls and predatory
situations, but such individual learning is potentially costly (Griffin
2004). The risks can be minimized by using information from
experienced companions. Such social learning is common in many
species when it comes to predator recognition (Cook & Mineka
1990; Griffin 2004; Shier & Owings 2007), and is also likely to play
a major role in the development of alarm call responses. For
example, during the first 3 months of age, meerkat pups mostly run
to the nearest adult when hearing an alarm call and can therefore
observe and follow the responses of the more experienced individuals (Hollén & Manser 2006). Those pups that do not run to an
adult are more likely to show adult-like responses if they first look
at an adult individual (see also Seyfarth & Cheney 1986; Fichtel
2008). In general, there is a strong tendency for young to start
responding in an adult-like fashion independently of others only
when they begin spending time away from adults (McCowan et al.
2001; Hollén & Manser 2006; Fichtel 2008).
Given that experience with social companions is evidently
important, there have been surprisingly few attempts to investigate
the extent to which learning is involved in the development of
alarm call responses. As with the study of alarm call usage, crossfostering is likely to be particularly beneficial in this regard, but
Davies and colleagues are the only researchers who have so far
L.I. Hollén, A.N. Radford / Animal Behaviour 78 (2009) 791–800
attempted this with respect to alarm calls. In one study they crossfostered newly hatched dunnocks, Prunella modularis, and robins,
Erithacus rubecula, and revealed that both species cease begging
only in response to conspecific alarm calls; they did not develop
this response to their foster species’ alarms, suggesting a strong
genetic basis (Davies et al. 2004). The response of cross-fostered
nestlings to conspecific calls was nevertheless weaker than that of
nestlings raised by their own species, showing that some learning is
necessary to fine-tune their natural responses (see also Madden
et al. 2005; Davies et al. 2006). Although cross-fostering is likely to
be easier in birds, studies on macaques have shown that it should
not be discounted as a possibility with certain mammals (see
Owren et al. 1993; Seyfarth & Cheney 1997).
There has also been little work on how neuroendocrine changes
can affect responsivity and learning in young animals. Studies
comparing developmental trajectories and response behaviours of
animals with different rearing histories would be invaluable in this
regard because early social experience is known to affect neural
development in the brain (e.g. Bredy et al. 2003), and particularly
the molecular and cellular organization of the fear circuit (see
Wiedenmayer 2009). Comparative research of this nature would
also enable an investigation of the extent to which auditory experience is needed for alarm call response development. To date, only
one such study has been conducted. Hauser (1988) compared wild
populations of the same species that were exposed to different
levels of alarm calls and predators and found that infant vervet
monkeys exposed to high rates of superb starling Spreo superbus,
alarm calls respond correctly to these calls earlier in development
than individuals exposed to calls at a lower rate. If such comparisons are not feasible because variability in exposure is either lacking or difficult to quantify, some viable alternatives include
providing groups of captive juveniles with different exposure levels
(see Mateo 1996a), comparing wild and captive populations of the
same species (although such different environments may confound
the results; Mateo & Holmes 1999a, b; Hollén & Manser 2007b), or
examining the behaviour of individuals in populations before and
after the introduction of novel predators or the reintroduction of
absent predators (Gil-da-Costa et al. 2003).
FUTURE DIRECTIONS
Despite the recent rapid increase in studies examining the
development of alarm call behaviour, there is still much that
remains unknown or unexplored. In addition to the suggestions
detailed above, the following topics have the potential to provide
particularly fruitful insights. First, all research on the development
of alarm call production has so far been conducted on nonhuman
primates and sciurids (see Table 1). This is particularly surprising
given the vast research literature on the development of birdsong
(reviewed in Catchpole & Slater 2008), and it is a shame that alarm
calls were never considered by isolation studies investigating avian
vocal development (e.g. Thorpe 1958; Morton et al. 1986; Hultsch &
Todt 1992). Whereas song development clearly involves learning
(Catchpole & Slater 2008), mammalian alarm calls seem to undergo
relatively minor modification during development (Blumstein &
Munos 2005; Randall et al. 2005; Hollén & Manser 2007a). Where
do bird calls fit in? Does their development follow the same
pathway as that of song or is it more similar to that of mammalian
alarm calls, thus being guided by similar processes across taxa?
Studies on the development of alarm call production in birds
should be easy to initiate because the required techniques, such as
the use of sophisticated acoustic analysis software, predator
presentations and cross-fostering, are already well established.
Moreover, the methods used to determine the neurological basis of
birdsong could be easily transferred to studies of alarm calls, thus
797
providing a novel insight into their development in this taxa and
more generally.
Second, although it is clear that learning is important for the
development of alarm call behaviour, especially usage and
responses, little work has attempted to tease apart the variety of
individual and social processes that might be involved (see Janik &
Slater 2000; Moore 2004; Dugatkin 2008). A few early studies that
tackled this issue reared young of social species in total isolation
(e.g. Herzog & Hopf 1984), but this method is ethically unsound and
leads to questionable conclusions because the individuals involved
are likely to display unnatural behaviours. To avoid these problems,
we suggest instead the use of temporary removals at different ages.
The isolated individuals could then be subjected to playbacks of
alarm calls or model predator presentations and if, for example,
they show appropriate responses, it suggests that they have
developed an association between an alarm call and a particular
response and/or context, rather than using cues given by adults or
the sight of predators (the development of alarm call usage could be
investigated in the same way). We also suggest that more simple
learning processes should not be ignored. For example, young could
cease responding to harmless stimuli through habituation, where
repeated exposure causes a decline in responsiveness because no
reinforcement follows (Thorpe 1963). Finally, it is worth noting that
development need not be constrained to young animals: individuals may continue to adjust their behaviour throughout life, to
changing circumstances. Different forms of learning may play a role
at different times, but this possibility has received no research
attention to date (Janik & Slater 2000).
The third major area we suggest for future consideration is the
use of false alarm calls (given when there is no imminent danger) to
gain an advantage in competitive interactions over food: if the
victim responds by fleeing to cover, the alarm caller can potentially
steal the food (Munn 1986; Ridley & Raihani 2007; Wheeler 2009).
Frequent false calling by kleptoparasites is likely to reduce their
effectiveness and the best rate might depend on, for example, the
particular habitat and thus the ease with which receivers can
identify whether a predator is actually present (Munn 1986). Young
kleptoparasites therefore need to learn at what rate to give true and
false alarm calls to be successful, but no studies have considered
how this behaviour develops. To minimize the cost of responding to
false alarm calls, host young also need to learn which heterospecific
species give false alarm calls, the rate at which they do so and hence
their relative level of unreliability, but how they do this has yet to
be explored. How members of one species assess the reliability of
individuals of another species would potentially help us understand the cognitive abilities underlying response behaviour and the
flexibility of specific learning processes.
CONCLUSIONS
In general, there are strikingly different developmental trajectories for the different aspects of alarm call behaviour. Alarm call
production undergoes relatively minor modification during development, appearing almost adult-like on first expression, and those
changes that do occur are likely to be the consequence of physical,
physiological and/or neurological maturation. In contrast, alarm
call responses often undergo more dramatic changes as individuals
grow older, and are more influenced by individual and/or social
experiences gathered during development. Alarm call usage
appears intermediate, with its development dependent on a mix of
genetic predispositions, neurological maturation and/or experience. Perhaps because of the ease with which playback experiments can be conducted to test for differences in alarm call
responses between adults and young, the majority of developmental studies have focused on this aspect of alarm call behaviour.
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L.I. Hollén, A.N. Radford / Animal Behaviour 78 (2009) 791–800
However, given that call production, usage and responses are
controlled by different causal mechanisms, detailed examinations
of all three aspects in the same species (so far only done in meerkats and vervet monkeys; Table 1) are vital.
Different species also vary greatly in the speed with which they
develop alarm call behaviour. In terms of alarm call responses, for
example, appropriate behaviour is apparent in some on first
exposure to danger, while in others it can take months before such
behaviour emerges. One reason for this is the sensitivity of
behavioural development to local environmental conditions, which
makes adaptive sense if factors that influence survival and reproduction differ from place to place or over time. Some differences
between species in the pattern of their developmental trajectories
might therefore be attributable to, for example, variation in the
intensity of predation experienced by young animals. The amount
of parental care provided is also likely to help explain interspecific
differences in developmental rates. For example, in those species in
which response patterns emerge over a long time, young seem to
converge on adult-like responses at approximately 6–7 months.
These species have in common that young are initially protected by
their mothers or other adults, and the expression of adult-like
behaviour seems to coincide with the point at which they start to
move around independently. Sufficient studies have potentially
been conducted on alarm call responses (although not the other
two aspects of alarm call behaviour) to consider meta-analyses,
thereby enabling us to acquire more powerful estimates of the true
effect sizes for the influence of such variables as age and social
experience.
Although it is very possible that in many cases the difference
in behaviour between juveniles and adults is because the former
have yet to acquire adult-like competence, it is equally plausible
that their behaviour is age adaptive and subsequent changes are
the result of, for example, a change in vulnerability or mobility. It
is therefore important that the results of studies investigating the
development of alarm call behaviour are subjected to interpretations from both the information transfer perspective and the
assessment–management viewpoint. It is also worth noting that if
we are interested in perceiver psychology, the assessment–
management framework puts much more emphasis on this than
the information transfer viewpoint; aspects of acoustic structure
that, for example, increase or decrease detectability, discriminability and memorability all become more relevant in the former
view. Although the two frameworks are by no means mutually
exclusive, it would be possible in many cases to set up competing
hypotheses to try to tease them apart. This does, however, require
experimental studies of the survival value of specific behaviours,
something that is currently lacking in the literature. By elucidating whether young behave in a way reflecting ontogenetic
adaptations or preparation for maturity, as well as broadening the
use of various techniques (e.g. cross-fostering, temporary
removals), forming stronger collaborative links with other disciplines (e.g. physiology, neurobiology) and initiating new avenues
of research (e.g. kleptoparasitism), research into the development
of alarm call behaviour will continue to play a key role in our
understanding of a wide variety of topics, including the evolution
of communication and language, kin selection and cognitive
processing.
Acknowledgments
We thank Nick Davies, Sarah Hodge, Joah Madden, Marta
Manser, Göran Spong and three anonymous referees for providing
constructive criticism and useful suggestions on earlier versions of
the manuscript. We also owe massive thanks to Louise Barrett for
her extensive help, encouragement and patience. L.I.H. was
supported by a Swiss National Science Foundation Fellowship and
a Marie Curie Fellowship, and A.N.R. by a BBSRC David Phillips
Fellowship.
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